Turkish Journal of Botany Turk J Bot (2013) 37: 894-907 http://journals.tubitak.gov.tr/botany/ © TÜBİTAK Research Article doi:10.3906/bot-1209-56

Floristic diversity and vegetation analysis of Wadi Al-Noman, Mecca, Saudi Arabia

1,2, 3,4 1 Kadry ABDEL KHALIK *, Mohamed EL-SHEIKH , Abeer EL-AIDAROUS 1 Biology Department, Faculty of Science, Umm-Al-Qura University, Mecca, Saudi Arabia 2 Botany Department, Faculty of Science, Sohag University, Sohag, 3 Botany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi Arabia 4 Botany Department, Faculty of Science, Damanhur University, Damanhur, Egypt

Received: 27.09.2012 Accepted: 14.03.2013 Published Online: 06.09.2013 Printed: 30.09.2013

Abstract: Wadi Al-Noman in Mecca is one of the most important wadis. It was included among the most important water sources where the springs and wells of Zobida run and it provides drinking water for the holy places in Mecca and visitors to the Kaaba and Arafat regions. The present study provides an analysis of floristic composition, vegetation types, and structure and species distribution at 20 sites, emphasising the environmental factors that affect species distribution. A total of 126 species representing 39 families of vascular are recorded. , Poaceae, and Boraginaceae are the largest families, and therophytes and chamaephytes are the most frequent, indicating a typical desert life-form spectrum. The floristic composition of the different geomorphologic landscape units shows differences in species richness. The highest species richness value (23 species stand–1) is recorded in the wadi bed. The lowest species richness value (18 species stand–1) is recorded in the wadi plateau and fissures. Chorological analysis revealed that 52% of the studied species are bioregional, native to the Saharo-Arabian–Sudano-Zambezian region. After application of the TWINSPAN, DCA, and CCA programs 4 vegetation groups were identified, and they were named after the characteristic species as follows: (I) Aristolochia bracteolata-Cucumis prophetarum; (II) Calotropis procera-Acacia hamulosa-Caralluma russeliana; (III) Acacia abyssinica- Acacia hamulosa-Tephrosia desertorum; and (IV) Argemone ochroleuca- italica. The associations and speciation of these Wadi Al- Noman plants demonstrate significant variation in pH, electrical conductivity, soil mineral contents, and human impact.

Key words: Floristic, canonical correspondence analysis, vegetation, multivariate analysis, wadi maturation, xerophytes

1. Introduction It is to be noted that the human activities in the Saudi Arabia is a huge arid desert with an area of about desert landscape have increased recently, due to rapid 2,250,000 km2 and covers the majority of the Arabian development in the study area. Human activities, through Peninsula. Therefore, xerophytic vegetation is a prominent their effect on the physical components of the fragile feature of the life in this country (Zahran, 1982). Wadis desert ecosystem, contribute to disruption of the natural represent one of the most prominent desert landforms, equilibrium among the components of the ecosystem. exhibiting physiographic irregularities that lead to parallel Usually, the main component subject to degradation is variation in species distribution (Kassas & Girgis, 1964). the soil, which is the basic resource of the ecosystem. This Life-form distribution is closely related to topography and inevitably results in retrogressive changes in the vegetation landform (Kassas & Girgis, 1965; Zohary, 1973; Orshan, (Shaltout & El-Sheikh, 2003; Guo, 2004). 1986; Fakhireh et al., 2012). Life-form composition is typical A number of studies were conducted in the past to of desert flora; the majority of species are therophytes and evaluate the life in deserts (Migahid, 1978; Chaudhary, chamaephytes. Wadi vegetation in general is not constant. 1999–2001) and they helped to strengthen the foundation It varies from year to year depending upon moisture levels of desert studies in Saudi Arabia. Al-Farraj et al. (1997) (Siddiqui & Al-Harbi, 1995). Establishment, growth, conducted vegetation studies in some raudhas in order regeneration, and distribution of the plant communities to verify the abundance, frequency, and density of each in the wadis are controlled by many factors such as species. A general description of the vegetation of western geographical position, physiographic features, and human Saudi Arabia was given by Vasey-Fitzeraid (1957a, 1957b), impact (Shaltout & El-Sheikh, 2003; Kürschner & Neef, and he recognised a number of vegetation and ecological 2011; Alatar et al., 2012; Korkmaz & Özçelik, 2013). types including littoral marshes, coastal desert plain, coastal * Correspondence: [email protected] 894 ABDEL KHALIK et al. / Turk J Bot foothills, mountain ranges, and wadis. Considerable efforts 2. Materials and methods have been made to interpret vegetation–environmental 2.1. Sample sites relationships in wadi ecosystems (Kassas & Imam, 1954, A total of 20 sample plots were selected along the Wadi 1959; Batanouny, 1979; El-Sharkawi et al., 1987; Shaltout Al-Noman under study (upstream, midstream, and & Mady, 1996; Al-Farhan, 2001; Alatar et al., 2012; Salama downstream parts, including the different wadi tributaries) et al., 2013). Some other reports have dealt with the in the period from January 2010 to January 2012. Locations vegetation types in certain regions of the Saudi Kingdom, and sample plots were selected to represent a wide range particularly in the Hijaz and Aseer regions (Zahran, 1982, of physiographic and environmental variation in each 1983; Batanouny & Baeshain, 1983; Abulfatih, 1992; tributary. In each location, sample plots were selected Abd El-Ghani, 1993; Fayed & Zayed, 1999; Al Wadie, randomly using the relevé method described by Muller- 2002; Fahmy & Hassan, 2005). Abdel-Fattah and Ali Dombois and Ellenberg (1974). The sample plots were (2005) indicated that soil water table and salinity cause 50 m × 50 m, and the sampling process was carried out discontinuities of vegetation in the Taif area (80–100 km during the spring season when most species were expected south-east of Mecca). Moreover, Parker (1991) showed to be growing (Figure 1). The vegetation sampling involved that water availability, including annual precipitation, soil listing all plant species at the sample plots. The plant cover properties, and topography, were biotic factors. In Mecca, of each species was estimated according to the Zurich- a few studies have provided qualitative valuations of the Montpellier technique (Braun-Blanquet, 1965). distribution of plant species and associations in relation to The collected plant specimens were identified and physiographic factors (Abd El-Ghani, 1993, 1997). named according to Collenette (1999), Cope (1985), Our aim is to analyse the vegetation of the Wadi Al- Mighaid (1996), and Chaudhary (1999–2001). Plant Noman in terms of species floristic composition, life-form, specimens were deposited in the Umm Al-Qura University chorotype, diversity, and community structure in relation Herbarium, Biology Department, Faculty of Science. to edaphic variables. We also provide a general description Species life-forms were determined according to the of the floristic and ecological features of the different location of regenerative buds and the parts shed during the habitats in the study area, which is considered one of the unfavourable season (Raunkier, 1934). A chronological most diverse sites in the Mecca strip, presumably due to analysis of the floristic categories of species was made to the greater amounts of run-off water collecting there. assign the recorded species to world geographical groups, 1.1. The study area according to Wickens (1978) and Zohary (1973). The city of Mecca lies in the western part of Saudi Arabia at 2.2. Soil analysis 21°26′N and 39°46′E, about 80 km from Jeddah on the Red Soil samples were collected at 3 random points from each Sea coast. It is bordered by almost continuous granite and site as a profile (composite samples) at a depth of 0–50 cm. granite gneiss ridges (Brown et al., 1962). Wadi Al-Noman The electrical conductivity (EC) and pH for each sample is also located in the western part of Saudi Arabia, between were determined as a 1:5 dilution in deionised water the El Hada mountains in the east and the Red Sea coast in (Wilde et al., 1979). Soil analyses including total dissolved the west, and it extends between 21°06′N and 21°32′N and –1 salts (TDS; g L ) and total carbonates (CO3), bicarbonate 39°32′E and 40°20′E (Figure 1). It covers an area of 740.1 (HCO ), and chlorides (Cl; g 100 g–1 DW) were analysed 2 3 km and extends about 25 km from Mecca. It is bordered to by precipitation by AgCl and titration according to Jackson the north by Wadi El-Begaedy, to the west by Wadi Orna, to –1 (1967); sulphates (SO4; g 100 g DW) were precipitated the south by mountains and Wadi Melcan, and to the east gravimetrically and estimated according to Wilde et al. by the El Hada mountains. The vegetation in this arid area (1979). Major cations such as sodium (Na), potassium (K), is of a restricted type (mode contracté, sensu Monod, 1954) calcium (Ca), and magnesium (Mg; g 100 g–1 DW) were and is found only in runnels, wadis, and depressions with determined in the 1:5 soil extract by flame photometer deep, fine sediments that receive an adequate water supply (Jenway, PFP-7), according to the methods of Williams and are mainly ground-water–dependent (Abd El-Ghani, and Twine (1960). The minor cations iron (Fe), copper 1992). According to Walter et al. (1975), the study area lies (Cu), and zinc (Zn) were determined using a GBC model within the subtropical dry zone and it has very hot summers 1100B atomic absorption spectrophotometer, and their and mild winters. The average annual temperature is 30.7 concentrations were expressed in mg kg–1 dry soil. °C; January is the coldest month with the lowest average 2.3. Data analysis temperature (23.9 °C), and the hottest month is July with Species cover-type data matrices were created as follows: the highest average temperature (35.8 °C) (Figure 2). (1) matrix of 20 sample plots × 100 common species cover Precipitation is scanty and unpredictable. The average values, and (2) matrix of 20 sample plots × 100 species cover annual precipitation is 9.2 mm, which usually falls during values and soil variables. For classification and ordination the winter months; however, the interannual variability of of the wadi vegetation, multivariate analyses were applied to rain is high, and extreme rainfall can be more than 100 mm.

895 ABDEL KHALIK et al. / Turk J Bot

MECCA

Figure 1. Map of study area Wadi Al-Noman showing sample plots 1–20.

40 80 Mecca (241 mm) 43.7 °C 155.2 mm classifies both stands and species directly, constructing an 1980-2007 (27 years) ordered 2-way table to exhibit the relationship between 35 70 them as clearly as possible. TWINSPAN produces a 30 60 hierarchical classification of vegetation groups (i.e. plant communities). Plant communities were named after their 25 50 dominant species. Detrended correspondence analysis Temp. °C (DCA) (Hill, 1979b) was applied to the same first matrix data 20 40 set in order to obtain an efficient graphical representation Ra nfall 15 30 of the ecological structure of vegetation groups identified using TWINSPAN and to verify the identified vegetation 10 20 units. In order to detect correlations between derived vegetation associations and environmental data, canonical 5 10 correspondence analysis (CCA) according to Ter Braak and 0 0 Smilauer (2002) was conducted with species cover, stands, JFMAMJ JASOND and soil variables using the second matrix (El-Sheikh et al., Figure 2. Climate diagram for Mecca, Saudi Arabia. 2010). Relationships between the ordination axes on one hand and community and soil variables on the other were tested using Pearson’s simple linear correlation coefficient the 2 data sets. The first matrix was subjected to numerical (r). Variation in species diversity, sample plot traits, and classification using 2-way indicator species analysis soil variables in relation to plant community were assessed (TWINSPAN) (Hill, 1979a). This procedure simultaneously using one-way analysis of variance (SAS, 1989–1996).

896 ABDEL KHALIK et al. / Turk J Bot

3. Results Ph 13%  32% 3.1. Floristic diversity Ph A total of 126 species belonging to 90 genera and 39 Ch families were recorded from various sample plots and H P 1% attached areas. The most highly represented families G were Poaceae (Gramineae) and Fabaceae (Leguminosae). P Chamaephytes constituted 50 species, or 40% of the total G 2% Ch 40%  species, followed by 40 species of therophytes (32%) and 16 species of phanerophytes (13%) (Table 1; Figure H 12% 3). Chronological analysis of the species in the study Figure 3. Life-form relative spectrum of Wadi Al-Noman area revealed that biregional elements that belong to the vegetation. Ch = chamaephyte, Th = therophyte, Ph = Saharo-Arabian and the Sudano-Zambezian together phanerophyte, H = hemicryptophyte, P = parasite, and G = have the highest share of species, representing 66 or geophyte.

Table 1. Synoptic table of species composition of the 4 vegetation groups (I–IV) identified after the application of TWINSPAN to the vegetation data of the 20 sample plots of Wadi Al-Noman region. Cover levels: 1, <10%; 2, 10%–20%; 3, 20%–30%; 4, 30%–40%; and 5, >40%. Vegetation groups: (I) Aristolochia bracteolata-Cucumis prophetarum, (II) Calotropis procera-Acacia hamulosa-Caralluma russeliana, (III) Acacia abyssinica-Acacia hamulosa-Tephrosia desertorum, and (IV) Argemone ochroleuca-Senna italica. Life-forms: Th = therophyte, Ch = chamaephyte, Ph = phanerophyte, He = hemicryptophyte, Cr = cryptophyte. Chorotypes: COSM = Cosmopolitan, Pal = Palaeotropical, Pan = Pantropical, SA = Saharo-Arabian, SZ = Sudano-Zambezian, ME = Mediterranean, and IT = Irano-Turanian.

Vegetation groups I II III IV TWINSPAN Taxa Life-form Chorotype 11 1 111 2 1111 levels 56233499456120780178 Ruellia patula Jacq. Ch ME + SA + SZ --33------00000 Achyranthes aspera L. Th IT + ME --3------00000 Acacia seyal Del. Ph SA + SZ --33------00000 Commicarpus helenae (J.A.Schultes) Meikle Ch SA + IT --34------00000 Pupalia lappacea (L.) Juss. Ch PAL (weed) --3------3------00001 Chenopodium murale L. Th COSM (weed) --3------3------00001 Seddera virgata Hochst. & Steud. Ch SZ ---3--3------00001 Solanum nigrum L. Ch COSM (weed) --3---3------00001 Glinus lotoides L. Th PAL (weed) ------33------000101 Amaranthus graecizans L. Th PAL (weed) ----3----33------000101 Amaranthus hybridus L. Th PAL (weed) ------43------000101 Trichodesma ehrenbergiana Schweinf. Ch SA + SZ ------3--3------000101 Senecio flavus (Decne.) Sch. Bip. Th SA + SZ ------3--33------000101 Pulicaria crispa (Forssk.)Benth. & Hook. Ch SA + SZ ------3---3------000101 Cuscuta hyalina Roth. P SA + SZ ------3-3------000101 Phyllanthus maderaspatensis L. Th PAL (weed) ------3--33------000101 Lavandula pubescens Decne. Ch SA + SZ ------33------000101 Ochradenus baccatus Delile Ph SA + SZ ---34-3--33------3-- 00011 Cucumis prophetarum L. H SA + SZ 43-3--3------001000 Phragmites australis (Cav.) Trin. ex Steud. G IT + ME + SA 4------001000 Aristolochia bracteolata Lam. Ch SA + SZ 43--33------001001

897 ABDEL KHALIK et al. / Turk J Bot

Table 1. (Continued).

Calendula arvensis L. Th PAN (weed) 3------33------001010 Cocculus pendulus (J.R.&G.Forst.) Diels Ph SA + SZ 33--3-333-3---3----- 001010 Leptadenia arborea (Forssk.) Schweinf. Ph SA + SZ 3---333------001011 Euphorbia arabica T.Anderson H ME + SA + SZ 3-3-3-3--33------001011 Indigofera spinosa Boiss. Ch SA + SZ 3334333-333-----3--- 001011 Portulaca oleracea L. Th COSM (weed) 3-3-333------001011 Blepharis ciliaris (L.) B.L.Burtt. Ch SA + SZ --3-3-3-33-3-----3-- 0011 Rhazya stricta Decne. Ch SA + SZ --3-3334-----4------0011 Caralluma russeliana (Courb. ex Brongn.) Cufod. Ch SA + SZ --4333-3333---33---- 0011 Cleome paradoxa R.Br. H SZ ------3-3----3------010 Cleome scaposa DC. Th SA + SZ --33------3------010 Schouwia purpurea (Forssk.) Schweinf. Ch SZ ------33-----3------010 Polypogon monspeliensis (L.) Desf. Th IT + ME + SA ---3---333----3---3- 010 Aerva javanica (Burm.F.) Juss. ex Schult. Ch SA + SZ 3-33----3333333----- 01100 Calotropis procera (Ait.) Ait.F. Ch SA + SZ 3-44434-444--4444--- 01100 Heliotropium strigosum Willd. Ch SA + SZ 3---3------3----- 01100 Trichodesma africana (L.) R.Br. Ch SA + SZ 33--3------3-3------01100 Aizoon canariense L. Th SA + SZ --3---3-33-433------01101 Tephrosia desertorum L. Ch SA ----333-434433333--- 01101 Acacia hamulosa Benth. Ph SA + SZ ----4334433333333--- 01101 Acacia asak (Forssk.) Willd. Ph SA + SZ ------343---44---- 01101 Aristida adscensionis L. Th SA --3-----3----3----3- 01110 Rumex vesicarius L. Th ME + SA + SZ --3-3------33 01110 Lycium shawii Roem. & Schult. Ph SA + SZ 3-33--3------33--3- 01110 Setaria viridis (L.) P.Beauv. Th IT + ME + SA 3--3---333----3---33 01111 Lindenbergia indica (L.) Kountze Th PAL (weed) 3------3------3- 01111 Cleome droserifolia (Forssk.) Delile H SA + SZ 3-33--3------33---33 1000 Gynandropsis gynandra (L.) Briq. Th PAL (weed) 3------3- 1000 Sisybrium erysimoides Desef. Th ME + SA + SZ 3-3------33 1000 Datura innoxia Mill. Ch SA --33--3------33---3- 1000 Morettia parviflora Boiss. Th SZ 3-----333--333--4-33 10010 Abutilon pannosum (G.Forst.) Schltdl. Ch SA ---3----3--3--3----3 10010 Pistacia khinjuk Stocks Ph SA + SZ 4------4-- 10011 Leptadenia pyrotechnica (Forssk.) Decne. Ph SA + SZ 33------3----3--- 10011 Avena fatua Th PAL (weed) 3-3------3-3------10011 Forsskaolea tenacissima L. H SA + SZ 3------33-33----3-- 10011 Nepeta deflersiana Schweinf. ex Hedge Ch SA ------3------3--- 101000 Chenopodium ambrosioides L. Th COSM (weed) ----3------3------101001 Chrozophora oblongifolia (Delile) Spreng. Ch IT + ME ------3--3---33----- 101001 Panicum turgidum Forssk. G SA + SZ ------3------3--- 101001 Corchorus antichorus (L.) Raeusch. Ch ME + SA + SZ ----3-3------33----- 101001 Heliotropium longiflorum Hochst. & Steud. Ch SA + SZ ----33------3-3-3- 10101

898 ABDEL KHALIK et al. / Turk J Bot

Table 1. (Continued).

Fagonia paulayana Wagner & Vierh. Ch SA + IT --1-3-3------3--33- 10101 Stipagrostis ciliata (Desf.) de Winter H IT + ME + SA ------4----33------1011 Senna holosericea (Fresen.) Greuter H SA + SZ ------4------3-3--- 1011 Ziziphus spina-christi (L.) Willd. Ph SA + SZ 3-----3------333---- 1011 Heliotropium arbainense Fresen. CH SA + SZ ----4---3-----333-33 1100 Abutilon fruticosum Guill. & Perr. CH SA + SZ --3------33 1100 Abutilon muticum (Del.) Webb. CH SA ------3------3----3- 1100 Boerhavia repens L. CH SA + SZ ------3------33 1100 Capparis spinosa L. Ch IT + ME ------33 110100 Malva parviflora L. Th IT + ME ------33 110100 Ficus salicifolia Vahl Ph SA + SZ ------33 110100 Argemone ochroleuca Sweet Th SA + SZ ------44 110100 Senna alexandrina Mill. H SA + SZ ------3333 110101 Tribulus pentandrus Forssk Th SA + SZ ------33- 110101 Cleome chrysantha Decne. Ch SA ------33-----33 11011 Senna italica Mill. H SA + SZ ------3------433-34 11011 Commicarpus plumbagineus (Car.) Standley Ch SA + IT ------3----4- 11011 Farsetia longisiliqua Decne. Ch SA + SZ ------3----3-3------11100 Solanum incanum L. Ch SA ------3------33----- 11100 Zygophyllum simplex L. Th SA + SZ ------3------3---3-- 11100 Convolvulus hystrix Vahl. H SA + SZ 3------33------11101 Cyperus rotundus L. G PAN (weed) 3------33---- 11101 Imperata cylindrica (L.) Raeusch. H PAN (weed) 3------3----3--- 11101 Tribulus macropterus Boiss. Th SA + SZ ---3------33-3-3--3 11101 Citrullus colocynthis (L.) Schrad. H Me + SA ------433333-34 11110 Schismus barbatus (L.) Thell. Th IT + ME + SA ------3-3-3- 11110 Aerva lanata (L.) Juss. ex J.A.Schultes Ch SA + SZ ------4--- 111110 Pergularia tomentosa L. Ch SA + SZ ------4----3--- 111110 Heliotropium pterocarpum Hochst. & Steud. Ch SA + SZ ------3--33-- 111110 Dipterygium glaucum Decne. Ch SZ ------4--33-- 111110 Cucumis dipsaceus Ehrenb. ex Spach H SA + SZ ------33-3-34-- 111110 Otostegia fruticosa (Forssk.) Schweinf. ex Penzig Ch SA ------33-- 111110 Tephrosia nubica (Boiss.) Baker Ch SA ------43-33---- 111110 Acacia abyssinica Hochst. Ph SA + SZ ------4334433-- 111110 Hyphaene thebaica (L.) Mart. Ph SA + SZ ------4------111110 Emex spinosus (L.) Campd. Th IT + ME + SA ------4----- 111110 Acacia elatior Brenan Ph SA + SZ ------3----4343----- 111111 00000000000111111111 00111111111000000011 0011111110000001 0001111000111 TWINSPAN level

899 ABDEL KHALIK et al. / Turk J Bot

52% of the total species, followed by the Saharo-Arabian the 20 Wadi Al-Noman sample plots, indicated 8 vegetation region elements at 12 (10%) and Palaeotropic at 9 (7%). subgroups at level 5, summarised into 4 vegetation Pluriregional elements that belong to the Saharo-Arabian, groups (VGs; i.e. plant communities) at level 2. These 4 Irano-Turanian, and Mediterranean regions and to the major plant communities were characterised and named Saharo-Arabian, Sudano-Zambezian, and Mediterranean after the dominant and subdominant species as follows: regions are represented by 8 and 7 species accounting (I) Aristolochia bracteolata-Cucumis prophetarum, (II) for 12% of the total species, respectively. The floristic Calotropis procera-Acacia hamulosa-Caralluma russeliana, composition of the study area also included 6 species in the (III) Acacia abyssinica-Acacia hamulosa-Tephrosia Sudano-Zambezian, 4 species in both the Irano-Turanian desertorum, and (IV) Argemone ochroleuca-Senna italic and Mediterranean, 4 in both the Saharo-Arabian and (Table 1; Figure 5). The application of DCA confirmed Irano-Turanian, 4 cosmopolitan species, 3 species in both the separation among these communities and indicated the Saharo-Arabian and Mediterranean, and 3 Pantropic some relationships between environmental gradients and species (Table 1; Figure 4). topographic aspects of Wadi Al-Noman (Figure 6). 3.2. Multivariate analysis CCA ordination was used to verify the correlation The application of TWINSPAN to the cover and presence analysis between the dominant environmental factors estimates of the 100 selected common species, recorded in and CCA axes. Correlation analysis indicated that the

%3 %3 COSM (weed) PAN ME+SA+SZ %5 %6 %3 %6 IT+ME SA PAL

%7 IT+ME+SA SA+IT SZ %52 %10 ME+SA SA+SZ %2

%3 Figure 4. Floristic category spectrum of Wadi Al-Noman. COSM = Cosmopolitan, PAL = Palaeotropical, PAN = Pantropical, SA = Saharo-Arabian, SZ = Sudano-Zambezian, Me = Mediterranean, and IT = Irano-Turanian. Ctrullu Indgofera spnosa Acaca abyssnc s colocynths Leptadena pyrotechnca Cappars spnosa a

Ruella patula Pstaca khnjuk

Leptadena arbore

Azoon canarens

a

e

(5,6) (12,13, 3,4,19 9,14,15,16) (1,2,20 7,8,10 11) (17,18) I II III IV Figure 5. The dendrogram illustrating the presence of 4 vegetation groups using TWINSPAN analysis of 20 sample plots in the study area.

900 ABDEL KHALIK et al. / Turk J Bot

1.5 AX2 separation of species along the first axis is affected negatively by K and species richness (–0.30) (Table 2). III 11 Therefore, Aristolochia bracteolata-Cucumis prophetarum 10 (VG I), which occupies the wadi plateau and fissures, and Calotropis procera-Acacia hamulosa-Caralluma russeliana 6 I 5 (VG II) and Acacia abyssinica-Acacia hamulosa-Tephrosia 4 1 desertorum (VG III), which occupy the wadi slope and 9 20 7 bed, were separated on the left of axis 1 from Argemone 8 2 ochroleuca-Senna italica (VG IV) on the right, which AX1 inhabits the wadi bed (Figure 7). 3 Xerophytes occupied the wadi hills and fissures of the flat stony habitat of the Aristolochia bracteolata-Cucumis 14 19 prophetarum VG I (e.g., Pistacia khinjuk, Leptadenia II pyrotechnica, Trichodesma africanum, Indigofera spinosa, 18 and Cocculus pendulus) on the upper, positive sector of axis 17 IV 2, and they are correlated with low species diversity and 16 13 soil mineral contents. The therophyte, chamaephyte, and 15 shrubs species of the Calotropis procera-Acacia hamulosa- 12 Caralluma russeliana VG II (e.g., Blepharis ciliaris, Aizoon –1.5 canariense, Aerva javanica, Rhazya stricta, Morettia parviflora, Euphorbia arabica, Phyllanthus maderaspatensis, Tephrosia desertorum, Cocculus pendulus, Ochradenus –1.5 2.0 baccatus, and Lycium shawii) on the centre and lower Figure 6. DCA ordination of the 4 vegetation groups identified negative part of axis 1 are related to high altitude, salinity, using TWINSPAN analysis of the 20 sample plots in the study and soil mineral contents. Ruderal and psammophytic area. species of the Argemone ochroleuca-Senna italica VG IV

Table 2. Interset correlations of environmental variables in Wadi Al-Noman with DCA axes. *: P ≤ 0.05. N Variable AX1 AX2 1 Alt (m) –0.2130 0.2282 2 pH 0.1169 –0.1696 3 EC (µS cm–1) –0.1224 –0.0016 4 TDS (ppm) –0.1205 –0.0369

5 CO3 (ppm –0.0792 –0.0632

6 HCO3 (ppm –0.0817 –0.0572

7 SO4 (ppm –0.0864 0.1580 8 Ca (ppm –0.0816 –0.0498 9 Na (ppm –0.1119 0.0733 10 K (ppm –0.30* 0.1669 11 Cl (ppm –0.1025 0.1502 12 Fe (ppm –0.1390 0.1216 13 Mg (ppm –0.1647 –0.0113 14 Total species (no.) 0.0178 –0.0391 15 Total cover (m 100 m–1) 0.0333 –0.1011 16 Simpson (C ) –0.30* –0.0360 17 Shannon Ĥ 0.1060 –0.1846

901 ABDEL KHALIK et al. / Turk J Bot

Figure 7. Transect diagram showing the topographic situation of the vegetation groups in the section part of Wadi Al-Noman. The vegetation groups are named as follows: (I) Aristolochia bracteolata-Cucumis prophetarum, (II) Calotropis procera-Acacia hamulosa- Caralluma russeliana, (III) Acacia abyssinica-Acacia hamulosa-Tephrosia desertorum, and (IV) Argemone ochroleuca-Senna italica. inhabit disturbed sample plots of the wadi bed (e.g., Citrullus Species richness was negatively correlated with Fe colocynthis, Heliotropium arbainense, Cleome chrysantha, (–0.50) and altitude (–0.33) (Table 3). Species cover was Cleome droserifolia, Morettia parviflora, Stipagrostis ciliate, positively correlated with pH (0.30) and species richness Senna alexandrina, Abutilon fruticosum, Malva parviflora, (0.98) and negatively with altitude (–0.31) and Fe (–0.54). Ficus salicifolia, and Boerhavia repens) on the positive part Species evenness was positively correlated with species of axis 1 and are related with high species diversity and richness, total plant cover, and pH (0.85, 0.87, and 0.41, plant cover values (Figure 8). respectively) and negatively with Fe (–0.40). 6

0. VG I

Ar br Ac se

In sp Alt Ar oc So Ly sh As ae K Cl 4 Fe Ca ru VG Ca pr Na II VG IV Rh st Zi sp EC Se il Mg TDS Total no. Ac ha Ac asCa Se ho Se al HCO3 T.spp. CO3 PH Te de Shannon Zy si Simpson Ac el ac ab Te nu VG III Cu di –0.6 –0.4 1.0 Figure 8. CCA biplot with environmental variables (arrows), the sample, and the abundant species represented by the first 2 letters of the genus and a specific epithet. For complete names of species, see Table 1.

902 ABDEL KHALIK et al. / Turk J Bot

Table 3. Correlation analysis (Pearson’s correlation coefficient = r) of species diversity and environmental variables. *: P ≤ 0.05, **: P ≤ 0.01, and ***: P ≤ 0.001.

Species richness Plant cover Conc. of dominance Relative evenness Variable (species stand–1) (m 100 m–1) (C) (Ĥ) Altitude (m) –0.33* –0.31* 0.24 –0.23 pH 0.22 0.30* –0.11 0.41** EC (µS cm–1) 0.11 0.11 –0.03 0.21 TDS (ppm) 0.10 0.13 0.01 0.22

CO3 (ppm) 0.12 0.18 –0.05 0.25

HCO3 (ppm) 0.12 0.18 –0.06 0.26

SO4 (ppm) 0.01 –0.02 –0.09 0.07 Ca (ppm) 0.19 0.20 –0.07 0.27 Na (ppm) –0.09 –0.06 0.06 –0.01 K (ppm) –0.07 –0.05 –0.01 0.03 Cl (ppm) –0.07 –0.08 0.03 –0.06 Fe (ppm) –0.50** –0.54** –0.21 –0.40** Mg (ppm) 0.17 0.17 –0.07 0.25 Species richness (species stand–1) 1.00 0.98*** –0.26 0.85*** Plant cover (m 100 m–1) 1.00 –0.15 0.87*** Conc. of dominance (C) 1.00 –0.12 Relative evenness (Ĥ) 1.00

3.3. Plant community–soil relationship species (10 and 11, respectively). A floristic analysis shows The Aristolochia bracteolata-Cucumis prophetarum that the majority of plants in the study area are annuals, and community (VG I) had the lowest species richness, plant the minority group occupies a tree habit. The dominance cover, relative species evenness, EC, TDS, CO3, HCO3, of members of Poaceae and Fabaceae coincides with the Ca, Na, and Cl values (18, 20, 1.12, 305, 199.7, 107.7, findings reported by Al-Turki and Al-Qlayan (2003), El- 109.5, 32.4, 15.1, and 2.5, respectively), whereas it had the Ghanem et al. (2010), and Alatar et al. (2012). The life-form highest Fe content (3.5) (Table 4). The Calotropis procera- distribution of plants growing in arid regions is closely Acacia hamulosa-Caralluma russeliana community (VG related to topography and landform (Kassas & Girgis,

II) achieved the highest altitude, EC, TDS, CO3, HCO3, 1964; Zohary, 1973; Orshan, 1986; Shaltout et al., 2010).

SO4, Ca, Na, K, Cl, and Mg values (649 m, 553, 288.7, 134, According to Walter et al. (1975), the study area lies within 137, 55, 61, 28.7, 12.7, 21, and 4.2, respectively) and had the subtropical dry zone, which has very hot summers and the lowest pH (7.24). On the other hand, the Argemone mild winters. The dominant perennial species provide the ochroleuca-Senna italica community (VG IV) demonstrated permanent character of the plant cover in each habitat. the highest levels of species richness (23), species cover (27 This may be credited to the rather short rainfall, which is m 100 m–1), species dominance (0.14), relative evenness not adequate for the appearance of many annuals. On the (1.33), and pH (7.37), whereas it had the lowest altitude, K, other hand, the rainy season provides a better opportunity Fe, and Mg levels (495 m, 6.7, 1.5, and 1.9, respectively). for the appearance of a considerable number of annuals, which then provide a characteristic physiognomy to the 4. Discussion vegetation (Hosni & Hegazy, 1996; Shaltout & Mady, 1996; In terms of floristic and vegetation composition in Shaltout et al., 2010; Alatar et al., 2012). the studied area, Poaceae (Gramineae) and Fabaceae The biological spectrum of the study area indicates (Leguminosae) are represented by the highest number of the dominance of chamaephytes (40%) and therophytes

903 ABDEL KHALIK et al. / Turk J Bot

Table 4. Mean ± standard error of soil variable and diversity indices of 4 vegetation groups after TWINSPAN as follows: (I) Aristolochia bracteolata-Cucumis prophetarum, (II) Calotropis procera-Acacia hamulosa-Caralluma russeliana, (III) Acacia abyssinica-Acacia hamulosa-Tephrosia desertorum, and (IV) Argemone ochroleuca-Senna italica. Maximum and minimum values in bold.

Variable VG I VG II VG III VG IV Mean F-value Species richness (species stand–1) 18.0 ± 12.0 22.4 ± 3.7 22.1 ± 3.4 23.0 ± 5.0 21.9 0.11 Total cover (m 100 m–1) 20.0 ± 14.0 25.3 ± 3.6 26.1 ± 4.1 27.0 ± 5.0 25.3 0.17 Conc. of dominance (C) 0.05 ± 0.04 0.07 ± 0.02 0.12 ± 0.03 0.14 ± 0.1 0.09 0.96 Relative evenness (Ĥ) 1.12 ± 0.34 1.24 ± 0.07 1.3 ± 0.05 1.33 ± 0.11 1.26 0.41 Altitude (m) 522.0 ± 2.0 648.78 ± 64.9 510.0 ± 17.9 495.0 ± 11.0 57.2 1.62 pH 7.30 ± 0.0 7.24 ± 0.12 7.29 ± 0.1 7.37 ± 0.1 7.28 0.13 EC (μS cm–1) 305.5 ± 7.5 552.8 ± 158.7 383.2 ± 46.4 352.6 ± 22.6 448.7 0.52 TDS (ppm) 199.7 ± 5.3 288.7 ± 70.2 248.7 ± 30.2 229.0 ± 14.7 233.0 0.60

CO3 (ppm) 107.7 ± 4.3 134.2 ± 26.9 118.0 ± 12.8 111.9 ± 3.8 123.7 0.18 109.5 ± HCO (ppm) 137.4 ± 27.7 119.9 ± 13.1 114.0 ± 4.0 126.2 0.19 3 4.5

SO4 (ppm) 35.3 ± 3.7 55.0 ± 16.7 31.0 ± 2.1 40.5 ± 0.5 43.17 0.64 Ca (ppm) 32.4 ± 1.6 61.1 ± 25.1 45.4 ± 8.4 38.3 ± 6.0 50.5 0.24 Na (ppm) 15.1 ± 0.2 28.7 ± 10.6 16.2 ± 1.8 18.5 ± 0.5 21.9 0.50 K (ppm) 7.4 ± 0.3 12.7 ± 2.1 8.1 ± 0.8 6.7 ± 3.1 9.9 1.75 Cl (ppm) 2.5 ± 0.0 21.2 ± 5.8 10.4 ± 2.1 3.5 ± 2.1 14.8 1.6 Fe (ppm) 3.5 ± 0.8 2.4 ± 1.2 1.8 ± 0.8 1.5 ± 0.8 2.2 0.23 Mg (ppm) 2.6 ± 0.0 4.2 ± 1.5 3.0 ± 0.3 1.9 ± 0.1 3.4 0.38

(32%). The domination of chamaephytes and therophytes interregional chorotype (mono- and pluriregionals) is not over other life-forms seems to be a response to the hot dry in accordance with Zohary (1973). The Saharo-Arabian– climate and human and animal interference. Therophytes Sudano-Zambezian chorotypes decrease moving north are adapted to the dryness of the region and shortage of and are replaced by Mediterranean and Irano-Turanian rainfall, because they spend their vegetative period in seed chorotypes (Danin & Plitman, 1987; Abd El-Ghani & form (Asri, 2003). These results are congruent with the Amer, 2003). This may be due to the fact that Saharo- spectra of vegetation in the desert habitats in other parts Arabian–Sudano-Zambezian and Saharo-Arabian plant of Saudi Arabia (El-Demerdash et al., 1995; Chaudhary, species are good indicators of a desert environment, while 1999–2001; Collenette, 1999; Al-Turki & Al-Qlayan, 2003; Mediterranean species point to a more mesic environment. Fahmy & Hassan, 2005; El-Ghanem et al., 2010; Alatar The low percentage of endemic species is remarkable. et al., 2012), and this picture also reflects the vegetation Wickens (1977) and Boulos (1997) mentioned that the spectra in other parts of the Middle East (Danin & Orchan, Saharo-Arabian region is characterised by the presence 1990; Zahran & Willis, 1992; Abd El-Ghani, 2000; El-Bana of few endemic species and genera. The Saharo-Arabian & Al-Mathnani, 2009). species that are restricted in their distribution to the The importance of the study area from a central strip of Saudi Arabia are more abundant in habitats phytogeographical point of view may be due to the with more favourable microenvironmental conditions and position of Mecca (Asir Mountains). Chorological analysis those providing better protection (Ghazanfar & Fisher, of the floristic data revealed that the Saharo-Arabian– 1998; Hegazy et al., 1998; El-Ghanem et al., 2010). Sudano-Zambezian chorotype (52%) forms the major Due to the sharp topography of the study area and component of the floristic structure in Wadi Al-Noman. the importance of this wadi, several microhabitats were The presence of the biregional Saharo-Arabian–Sudano- recognised, namely wadi beds, slopes, and cliffs. Each of Zambezian chorotype in a higher percentage than the these habitats supports a special type of vegetation with a

904 ABDEL KHALIK et al. / Turk J Bot characteristic floristic composition and plant cover. Wadi Al-Noman, which may be due to the similarities in climate Al-Noman in Mecca is one of the most important wadis. It and topography. VG I includes Aristolochia bracteolata- is a mature wadi characterised by its wide, deep valley fill Cucumis prophetarum and inhabits rocky outcrop slopes, deposits and well-defined canals cutting into older, rocky which consist of notches and shallow drainage runnels and limestone formations. Therefore, the wadi ecosystem can have low species diversity and plant cover (Kürschner & be divided into a distinct number of habitats according to Neef, 2011; Alatar et al., 2012). soil thickness and plant cover. Spatial distribution of plant The Acacia abyssinica-Acacia hamulosa-Tephrosia species and communities over a small geographic area in desertorum community of cliff, chasmophytic, shrubby, desert ecosystems is related to heterogeneous topography and grassy species inhabits the outcrops of the rocky and landform patterns (Kassas & Batanouny, 1984; Alatar slopes. Then comes the community of Calotropis procera- et al., 2012). The heterogeneity of local topography, Acacia hamulosa-Caralluma russeliana, composed of edaphic factors, and microclimatic conditions leads to dense, woody, and sparse short-lived annual species that variation in the distributional behaviour of the plant inhabit the main wide channel of the wadi bed. The most associations of the study area. In terms of classification, the diverse groups, VG II and VG III, inhabiting the wadi slope vegetation that characterises the study area can be divided outcrops and beds and characterised by Acacia hamulosa into 4 vegetation groups. Most of the identified vegetation and Acacia abyssinica-Calotropis procera, could be related groups are more or less comparable with those recorded in to higher concentration of salinity and soil mineral some other wadis of Saudi Arabia (Abd El-Ghani, 1997; Al contents, perhaps due to animal grazing, rainfall, and Wadie, 2002; Alatar et al., 2012) and the Taif region (Abdel floods and their effects on the parent rocks (Pulford et al., Fattah & Ali, 2005; Mosallam, 2007). 1992). The soil, accumulated by runoff water, supported Among these groups in the Wadi Al-Noman ecosystem, dense woody vegetation and grasses with dense cover VG IV, characterised by the Argemone ochroleuca-Senna during the rainy season. Similar conclusions were made italica community, has a clear difference from other by other authors (Chaudhary, 1983; El-Demerdash et al., groups; this community was recognised as pure vegetation 1995; Shaltout & Madi, 1996; Al-Yemeni, 2001; Abbadi & in the Sudera-Taif region by Mosallam (2007). This group El-Sheikh, 2002; Al Wadie, 2002; Springuel et al., 2006; Alatar et al., 2012). has the highest number of ruderals, weeds, and invasive A correlation analysis in the present study indicates that plant species (the plants that usually invade disturbed the species diversity (richness and evenness) is positively sites). This could be an effect of severe human impact, as correlated with increasing cover and pH. These factors may the wadi bed habitat has been subjected to intensive human reflect the human impact degree in some disturbed sites practices such as cutting, over-grazing, and construction of the wadi bed in the study area (e.g., VG IV, Argemone activities, especially roads. This is consistent with studies ochroleuca). In such cases, most of the total cover is indicating that the vegetation of intensively disturbed sites accounted for by 1 or 2 species that can make the best use is dominated by nonnative alien species and many annuals of available resources as a result of their high competitive and, therefore, has high species richness and plant cover capacities under environmental stress. Similar correlations (Shaltout & El-Sheikh, 2003; Kürschner & Neef, 2011; were reported by El-Demerdash et al. (1995), Abbadi and Alatar et al., 2012). On the other hand, VG II and VG III El-Sheikh (2002), El-Sheikh et al. (2006, 2010), and Alatar are less distinct because they are characterised by mixed et al. (2012). Concerning the socioeconomic changes of communities of native trees, shrubs, and grasses. In Saudi the wadi bed area, increasing human activities could be Arabia, Shaltout and Mady (1996), Abd El-Ghani (1997), observed. Such activities greatly change the community Al-Yemeni and Zayed (1999), Al-Yemeni (2001), Al- structure, species diversity, and plant cover (Batanouny, Wadie (2002), El-Ghanem (2006), and Alatar et al. (2012) 1987; Shaltout & El-Sheikh, 2003). recognised several plant associations, some of which are comparable to those of the present study (e.g., Acacia taxa, Acknowledgements Rhazya stricta), which are comparable to those identified We would like to thank Prof Dr van der Maesen, professor in neighbouring countries (Batanouny, 1987; El-Bana & of plant in the Biosystematics Group, Plant Al-Mathnani, 2009; Shaltout et al., 2010). Communities Science, Wageningen University, the Netherlands, for on stony plateaus and rocky outcrop slopes in Wadi Talha reviewing the manuscript. We are also grateful to the at Asir (Al-Wadie, 2002) and vegetation in Taif (Abdel Centre for Excellence in Biodiversity, King Saud University, Fattah and Ali, 2005) are, however, comparable to Wadi for supporting this vegetation diversity analysis research.

905 ABDEL KHALIK et al. / Turk J Bot

References

Abbadi GA & El-Sheikh MA (2002). Vegetation analysis of Failaka Boulos L (1997). Endemic flora of the Middle East and North Africa. Island (Kuwait). Journal of Arid Environments 50: 153–165. In: Barakat HN & Hegazy AK (eds.) Reviews in Ecology: Desert Abd El-Ghani M (1992). Flora and vegetation of Qara Oasis, Egypt. Conservation and Development, pp. 229–260. Cairo: Metropole. Phytocoenologia 21: 1–14. Braun-Blanquet J (1965). Plant Sociology: The Study of Plant Communities. New York: Hafner Publication Company. Abd El-Ghani M (1993). Habitat features and plant communities of the Holy Places, Makkah, Saudi Arabia. Feddes Repertorium Brown GF, Jackson RO, Boude RG & Maclean WH (1962). Geology 104: 417–425. of the Northern Hijaz Quadrangles, Kingdom of Saudi Arabia. Riyadh: Ministry of Petroleum and Mineral Resources, Saudi Abd El-Ghani M (1997). Phenology of ten common plant species in Arabia and Department of Interior, USGS. western Saudi Arabia. Journal of Arid Environments 35: 673– 683. Chaudhary SA (1983). Vegetation of the great Nafud, Saudi Arabia. National History Society 2: 32–37. Abd El-Ghani M (2000). Floristic and environmental relations in two extreme desert zones of western Egypt. Global Ecology and Chaudhary SA (1999–2001). Flora of the Kingdom of Saudi Arabia, Biogeography 9: 499–516. Vols. 1–3, Riyadh: Ministry of Agriculture and Water Press. Abd El-Ghani M & Amer WM (2003). Soil-vegetation relationships Collenette S (1999). Wild Flowers of Saudi Arabia. Riyadh: National in a coastal desert plain of southern Sinai, Egypt. Journal of Commission for Wild Life Conservation and Development. Arid Environments 55: 607–628. Cope T (1985). A Key to the Grasses of the Arabian Peninsula. Riyadh: Abdel-Fattah RI & Ali AA (2005). Vegetation environment Arab Bureau of Education for the Gulf States. relationships in Taif, Saudi Arabia. International Journal of Danin A & Orchan AG (1990). The distribution of Raunkiaer life Botany 1: 206–211. forms in Israel in relation to environment. Journal of Vegetation Science 1: 41–48. Abulfatih HA (1992). Vegetation zonation along an altitudinal gradient between sea level and 3000 meters in southwestern Danin A & Plitman U (1987). Revision of the plant geographical Saudi Arabia. Journal of King Saud University 4: 57–97. territories of Israel and Sinai. Plant Systematics and Evolution 156: 43–53. Alatar A, El-Sheikh MA & Thomas J (2012). Vegetation analysis of Wadi Al-Jufair, a hyper-arid region in Najd, Saudi Arabia. El-Bana MI & Al-Mathnani A (2009). Vegetation–soil relationships Saudi Journal of Biological Sciences 19: 357–368. in the Wadi Al-Hayat area of the Libyan Sahara. Australian Journal of Basic Applied Science 3: 740–747. Al-Farhan AH (2001). A floristic account on Raudhat Khuraim, Central Province, Saudi Arabia. Saudi Journal of Biological El-Demerdash MA, Hegazy AK & Zilay MA (1995). Vegetation soil Sciences 8: 80–103. relationships in Tihamah coastal plains of Jazan region. Saudi Arabia. Journal of Arid Environments 30: 161–174. Al-Farraj MM, Al-Farhan A & Al-Yemeni M (1997). Ecological studies on rawdhat system in Saudi Arabia I. Rawdhat Khorim. El-Ghanem WA, Hassan LM, Galal TM & Badr A (2010). Floristic Journal of Botany 29: 75–88. composition and vegetation analysis in Hail region north of central Saudi Arabia. Saudi Journal of Biological Sciences 17: Al-Turki TA & Al-Qlayan HA (2003). Contribution to the flora of 119–128. Saudi Arabia: Hail region. Saudi Journal of Biological Sciences 10: 190–222. El-Sharkawi HM, Salama PM & Fayed AA (1987). Vegetation of inland desert wadis in Egypt. 8: Vegetation of Wadi Kharit. Al Wadie H (2002). Floristic composition and vegetation of Wadi Feddes Repertorium 98: 543–547. Talha, Asser Mountains, South West Saudi Arabia. Journal of El-Sheikh MA, Abbadi GA & Bianco P (2010). Vegetation ecology of Biological Sciences 2: 285–288. phytogenic hillocks (nabkhas) in coastal habitats of Jal Az-Zor Al-Yemeni MN (2001). Ecology of some plant communities in Wadi National Park, Kuwait. Flora 205: 832–840. Al-Ammaria, Riyadh, Saudi Arabia. Saudi Journal of Biological El-Sheikh MA, El-Ghareeb RM & Testi A (2006). Diversity of Sciences 8: 145–165. plant communities in coastal salt marshes habitat in Kuwait. Al-Yemeni MN & Zayed KM (1999). Ecology of some plant Rendiconti Fisiche Accademia Lincei 17: 311–331. communities along Riyadh-Al-Thumamah Road, Saudi Fahmy AG & Hassan LM (2005). Plant diversity of Wadi el Ghayl, Arabia. Saudi Journal of Biological Sciences 6: 9–26. Aseer Mountains, Saudi Arabia. Egyptian Journal of Desert Asri Y (2003). Plant Diversity in Touran Biosphere Reservoir, No. Research 55: 39–52. 305. Tehran: Publishing Research Institute of Forests and Fakhireh A, Ajorlo M, Shahryari A, Mansouri S, Nouri S & Rangeland. Pahlavanravi A (2012). The autecological characteristics of Batanouny KH (1979). The desert vegetation in Egypt. Cairo Desmostachya bipinnata in hyper-arid regions. Turkish Journal University African Studies Revue 1: 9–37. of Botany 36: 690–696. Batanouny KH (1987). Current knowledge of plant ecology in the Fayed A & Zayed K (1999). Vegetation along Makkah-Taif road Arab Gulf countries. Catena 14: 291–316. (Saudi Arabia). Arabian Gulf Journal of Science Research 7: 97–117. Batanouny KH & Baeshin NA (1983). Plant communities along Medina–Badr road across the Hejaz Mountains, Saudi Arabia. Ghazanfar SA & Fisher M (1998). Vegetation of the Arabian Peninsula. Vegetatio 53: 33–43. London: Kluwer.

906 ABDEL KHALIK et al. / Turk J Bot

Guo Q (2004). Slow recovery in desert perennial vegetation following Salama F, Abd El-Ghani M & El-Tayeh N (2013). Vegetation and soil prolonged human disturbance. Journal of Vegetation Science relationships in the inland wadi ecosystem of central Eastern 15: 757–762. Desert, Egypt. Turkish Journal of Botany 37: 489–498. Hegazy AK, El-Demerdash MA & Hosni HA (1998). Vegetation, SAS (1989–1996). SAS/STAT User’s Guide. Cary, NC, USA: SAS species diversity and floristic relations along an altitudinal Institute Inc. gradient in south-west Saudi Arabia. Journal of Arid Environments 38: 3–13. Shaltout KH & El-Sheikh MA (2003). Vegetation of the urban habitats in the Nile Delta region, Egypt. Urban Ecosystems 6: Hosni HA & Hegazy AK (1996). Contribution to the flora of Asir, 205–221. Saudi Arabia. Candollea 51: 169–202. Shaltout KH & Mady MA (1996). Analysis of raudhas vegetation in Jackson ML (1967). Soil Chemical Analysis. New Delhi: Prentice Hall of India. central Saudi Arabia. Journal of Arid Environments 34: 441– 454. Kassas M & Batanouny KH (1984). Plant ecology. In: Cloudsley- Thompson JJ (ed.) Sahara Desert: Key Environments, pp. 77– Shaltout KH, Sheded MG & Salem AM (2010). Vegetation spatial 90. Oxford: Pergamon Press. heterogeneity in a hyper arid Biosphere Reserve area in north Africa. Acta Botanica Croatia 69: 31–46. Kassas M & Girgis WA (1964). Habitat and plant communities in the Egyptian desert. V. The limestone plateau. Journal of Ecology Siddiqui AQ & Al-Harbi AH (1995). A preliminary study of the 52: 107–119. ecology of Wadi Hanifah stream with reference to animal Kassas M & Girgis WA (1965). Habitat and plant communities in the communities. Arab Gulf Journal Science Research 13: 695–717. Egyptian desert. VI. The units of a desert ecosystem. Journal of Springuel I, Sheded M, Darius F & Bornkamm R (2006). Vegetation Ecology 53: 715–728. dynamics in an extreme desert wadi under the influence of Kassas M & Imam M (1954). Habitat and plant communities in episodic rainfall. Polish Botanical Studies 22: 459–472. the Egyptian desert. III. The wadi bed ecosystem. Journal of Ter Braak CFG & Smilauer P (2002). CANOCO Reference Manual Ecology 42: 242–441. and CanoDraw for Window’s User’s Guide: Software for Kassas M & Imam M (1959). Habitat and plant communities in the Canonical Community Ordination (Version 4.5). Ithaca, NY, Egyptian desert. IV. The gravel desert. Journal of Ecology 47: USA: Microcomputer Power. 289–310. Vesey-Fitzgerald DF (1957a). The vegetation of the Red Sea coast Korkmaz M & Özçelik H (2013). Soil-plant relations in the annual north of Jeddah, Saudi Arabia. Journal of Ecology 45: 547–562. Gypsophila (Caryopyhllaceae) taxa of Turkey. Turkish Journal of Botany 37: 85–98. Vesey-Fitzgerald DF (1957b). The vegetation of central and eastern Arabia. Journal of Ecology 45: 779–798. Kürschner H & Neef R (2011). A first synthesis of the flora and vegetation of the Tayma oasis and surroundings (Saudi Arabia). Walter H, Harnickell E & Mueller-Dombois D (1975). Climate Plant Diversity Evolution 129: 27–58. Diagram Maps. Berlin: Springer Verlag. Migahid AM (1996). Flora of Saudi Arabia, Vols. I–III. Jeddah: King Wickens GE (1977). Some of the phytogeographical problems Abdul Aziz University Press. associated with Egypt. Publications Cairo University Herbarium Mosallam HA (2007). Comparative study on the vegetation of 7–8: 223–230. protected and non-protected areas, Sudera, Taif, Saudi Arabia. Wickens GE (1978). The flora of Jebel Marra ( Republic) and its International Journal of Agriculture and Biology 9: 202–214. geographical affinities. Kew Bulletin Additional Series: 5–385. Monod T (1954). Mode contracté et diffuse de la vegetation Wilde SA, Corey RB, Lyer JG & Voigt GK (1979). Soil and Plant Saharienne. In: Cloudsley-Thompson JL (ed.) Biology of Analysis for Tree Culture. New Delhi: Oxford & IBH Publication Deserts, pp. 35–44. London: Institute of Biology. Co. Muller-Dombois D & Ellenberg H (1974). Aims and Methods of Williams V & Twine S (1960). Flame photometric method for Vegetation Ecology. New York: John Wiley and Sons. sodium, potassium and calcium. In: Peach K & Tracey MV Orshan G (1986). The desert of the Middle East. In: Evenari M, Noy- (eds.) Modern Methods of Plant Analysis, Vol. 5, pp. 3–5. Berlin: Meir I & Goodall DW (eds.) Ecosystems of the World, Vol. 12B, Springer Verlag. pp. 1–28. Amsterdam: Elsevier. Zahran M (1982). Vegetation Types of Saudi Arabia. Jeddah: King Parker K (1991). Topography, substrate, and vegetation patterns Abdel Aziz University Press. in the northern Sonoran Desert. Journal of Biogeography 18: 151–163. Zahran M (1983). Introduction to Plant Ecology and Vegetation Types Pulford ID, Murphy KJ, Dickinson G, Briggs JA & Springuel I (1992). in Saudi Arabia. Jeddah: King Abdul Aziz University Press. Ecological resources for conservation and development in Zahran M & Willis A (1992). The Vegetation of Egypt. London: Wadi Allaqi, Egypt. Botanical Journal of the Linnaean Society Chapman and Hall. 108: 131–141. Zohary M (1973). Geobotanical Foundations of the Middle East. Raunkiaer C (1934). Life Forms of Plants and Statistical Plant Stuttgart: Gustav Fischer Verlag. Geography. Oxford: Clarendon Press.

907